The bacteriophage T4 has long served as a model for the study of DNA replication, transcription, and recombination, and its relatively small size and well defined biochemistry make it an excellent model organism in which to integrate in vitro biochemistry into a chromosomal context. As a first step in characterizing the dynamics of chromosomal transactions during T4 infection, we employed a unique set of macro array strategies to identify the origins of viral DNA synthesis and monitor the actual accumulation of nascent DNA across the genome in real time. We have found that T4 DNA synthesis originates from at least five discrete loci within a single population of infected cells, near oriA, oriC, oriE, oriF, and oriG. This is the first direct evidence of multiple active origins within a single population of T4-infected cells, and it implies that T4 will provide insights into other multi-origin systems, like humans. The nascent DNAs produced from origin loci are regulated spatially and temporally, leading to the accumulation of multiple, short DNAs near the origins, which are later extended to full length genomes. This pattern of replication appears pivotal to the chromosome function, and mutations that alter replication dynamics also alter transcription patterns across the genome, suggesting that the two processes are dependent on one another. Indeed, when transcription is prevented at later times during infection, the origins used to initiate replication change. Presumably this interplay between replication and transcription has shaped the T4 genome, and our work provides the foundation for the future characterization of the molecular dynamics that contribute to T4 genome function and provide insights into the evolution of multi origin chromosomes.